Subtilisin-like proprotein convertase expression, localization, and activity in the human retina and optic nerve head

Investigative Ophthalmology and Visual Science

Volumn 50, Issue 12, 2009, Pages 5759-5768

  Fuller, John A ^a   Brun Zinkernagel, Anne Marie ^a   Clark, Abbot F ^a   Wordinger, Robert J ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOENZYME; MESSENGER RNA; PROTEIN PACE4; PROTEIN PC1; PROTEIN PC2; SERINE PROTEINASE; SUBTILISIN LIKE PROPROTEIN CONVERTASE; UNCLASSIFIED DRUG; PCSK6 PROTEIN, HUMAN; PRIMER DNA; PROPROTEIN CONVERTASE 1; PROPROTEIN CONVERTASE 2;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; GLIA; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; OPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RETINA NERVE CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ADULT; AGED; CHEMISTRY; ENZYMOLOGY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; MIDDLE AGED; OPTIC DISK; PHYSIOLOGY;

ADULT; AGED; AGED, 80 AND OVER; BLOTTING, WESTERN; DNA PRIMERS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; ISOENZYMES; MALE; MIDDLE AGED; OPTIC DISK; PROPROTEIN CONVERTASE 1; PROPROTEIN CONVERTASE 2; PROPROTEIN CONVERTASES; RETINA; RETINAL NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERINE ENDOPEPTIDASES;

EID: 73349138899     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.08-2616     Document Type: Article

References (83)

1. Quigley HA, Addicks EM, Green WR, Maumenee AE. Optic nerve damage in human glaucoma. II. the site of injury and susceptibility to damage. Arch Ophthalmol. 1981;99:635-649.
2. Hernandez MR, Andrzejewska WM, Neufeld AH. Changes in the extracellular matrix of the human optic nerve head in primary open-angle glaucoma. Am J Ophthalmol. 1990;109:180-188.
3. Morrison JC, Dorman-Pease ME, Dunkelberger GR, Quigley HA. Optic nerve head extracellular matrix in primary optic atrophy and experimental glaucoma. Arch Ophthalmol. 1990;108:1020-1024.
4. Orgul S, Cioffi GA, Wilson DJ, Bacon DR, Van Buskirk EM. An endothelin-1 induced model of optic nerve ischemia in the rabbit. Invest Ophthalmol Vis Sci. 1996;37:1860-1869.
5. Osborne NN, Ugarte M, Chao M, et al. Neuroprotection in relation to retinal ischemia and relevance to glaucoma. Surv Ophthalmol. 1999;43(Suppl 1):S102-S128.
6. Vorwerk CK, Lipton SA, Zurakowski D, Hyman BT, Sabel BA, Dreyer EB. Chronic low-dose glutamate is toxic to retinal ganglion cells. toxicity blocked by memantine. Invest Ophthalmol Vis Sci. 1996;37:1618-1624.
7. Quigley HA, McKinnon SJ, Zack DJ, et al. Retrograde axonal transport of BDNF in retinal ganglion cells is blocked by acute IOP elevation in rats. Invest Ophthalmol Vis Sci. 2000;41:3460-3466.
8. Quigley HA, Flower RW, Addicks EM, McLeod DS. The mechanism of optic nerve damage in experimental acute intraocular pressure elevation. Invest Ophthalmol Vis Sci. 1980;19:505-517.
9. Seidah NG, Chretien M, Day R. The family of subtilisin/kexin like pro-protein and pro-hormone convertases: Divergent or shared functions. Biochimie (Paris). 1994;76:197-209.
10. Seidah NG, Chretien M. Eukaryotic protein processing: endopro-teolysis of precursor proteins. Curr Opin Biotechnol. 1997;8:602-607.
11. Fuller RS, Brake AJ, Thorner J. Intracellular targeting and structural conservation of a prohormone-processing endoprotease. Science. 1989;246:482-486.
12. Mizuno K, Nakamura T, Ohshima T, Tanaka S, Matsuo H. Yeast KEX2 genes encodes an endopeptidase homologous to subtilisin-like serine proteases. Biochem Biophys Res Commun. 1988;156: 246-254.
13. Mbikay M, Tadros H, Ishida N, et al. Impaired fertility in mice deficient for the testicular germ-cell protease PC4. Proc Natl Acad Sci USA. 1997;94:6842-6846.
14. Marandi M, Mowla SJ, Tavallaei M, Yaghoobi MM, Jafarnejad SM. Proprotein convertases 1 and 2 (PC1 and PC2) are expressed in neurally differentiated rat bone marrow stromal stem cells (BMSCs). Neurosci Lett. 2007;420:198-203.
15. Seidah NG, Marcinkiewicz M, Benjannet S, et al. Cloning and primary sequence of a mouse candidate prohormone convertase PC1 homologous to PC2, furin, and Kex2: Distinct chromosomal localization and messenger RNA distribution in brain and pituitary compared to PC2. Mol Endocrinol. 1991;5:111-122.
16. Zhou A, Mains RE. Endoproteolytic processing of proopiomelano-cortin and prohormone convertases 1 and 2 in neuroendocrine cells overexpressing prohormone convertases 1 or 2. J Biol Chem. 1994;269:17440-17447.
17. Schafer MK, Day R, Cullinan WE, Chretien M, Seidah NG, Watson SJ. Gene expression of prohormone and proprotein convertases in the rat CNS: A comparative in situ hybridization analysis. J Neuro-sci. 1993;13:1258-1279.
18. Winsky-Sommerer R, Benjannet S, Rovere C, et al. Regional and cellular localization of the neuroendocrine prohormone converta-ses PC1 and PC2 in the rat central nervous system. J Comp Neurol. 2000;424:439-460.
19. Bruzzaniti A, Goodge K, Jay P, et al. PC8 [corrected], a new member of the convertase family. Biochem J. 1996:314:727-731.
20. Nagamune H, Muramatsu K, Akamatsu T, et al. Distribution of the kexin family proteases in pancreatic islets: PACE4C is specifically expressed in B cells of pancreatic islets. Endocrinology. 1995;136: 357-360.
21. Tsuji A, Mori K, Hine C, Tamai Y, Nagamune H, Matsuda Y. The tissue distribution of mRNAs for the PACE4 isoforms, kexin-like processing protease: PACE4C and PACE4D mRNAs are major transcripts among PACE4 isoforms. Biochem Biophys Res Commun. 1994;202:1215-1221.
22. Pearton DJ, Nirunsuksiri W, Rehemtulla A, Lewis SP, Presland RB, Dale BA. Proprotein convertase expression and localization in epidermis: evidence for multiple roles and substrates. Exp Derma-tol. 2001;10:193-203.
23. Bassi DE, Fu J, de Lopez Cicco R, Klein-Szanto AJ. Proprotein convertases: "master switches" in the regulation of tumor growth and progression. Mol Carcinog. 2005;44:151-161.
24. Akamatsu T, Matsuda Y, Tsumura K, et al. Highly regulated expression of subtilisin-like proprotein convertase PACE4 (SPC4) during dentinogenesis. Biochem Biophys Res Commun. 2000;272:410-415.
25. Akamatsu T, Purwanti N, Karabasil MR, et al. Temporospatially regulated expression of subtilisin-like proprotein convertase PACE4 (SPC4) during development of the rat submandibular gland. Dev Dyn. 2007;236:314-320.
26. Dong W, Marcinkiewicz M, Vieau D, Chretien M, Seidah NG, Day R. Distinct mRNA expression of the highly homologous converta-ses PC5 and PACE4 in the rat brain and pituitary. J Neurosci. 1995;15:1778-1796.
27. Zheng M, Seidah NG, Pintar JE. The developmental expression in the rat CNS and peripheral tissues of proteases PC5 and PACE4 mRNAs: comparison with other proprotein processing enzymes. Dev Biol. 1997;181:268-283.
28. Seidah NG, Benjannet S, Pareek S, et al. Cellular processing of the nerve growth factor precursor by the mammalian pro-protein convertases. Biochem J. 1996;314:951-960.
29. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGFbeta activation. J Cell Sci. 2003;116:217-224.
30. Seidah NG, Benjannet S, Pareek S, Chretien M, Murphy RA. Cellular processing of the neurotrophin precursors of NT3 and BDNF by the mammalian proprotein convertases. FEBS Lett. 1996;379:247-250.
31. Marcinkiewicz M, Marcinkiewicz J, Chen A, Leclaire F, Chretien M, Richardson P. Nerve growth factor and proprotein convertases furin and PC7 in transected sciatic nerves and in nerve segments cultured in conditioned media: their presence in schwann cells, macrophages, and smooth muscle cells. J Comp Neurol. 1999;403: 471-485.
32. Lissitzky JC, Luis J, Munzer JS, et al. Endoproteolytic processing of integrin pro-alpha subunits involves the redundant function of furin and proprotein convertase (PC) 5A, but not paired basic amino acid converting enzyme (PACE) 4, PC5B or PC7. Biochem J. 2000;346:133-138.
33. Seidah NG, Prat A. Precursor convertases in the secretory pathway, cytosol and extracellular milieu. Essays Biochem. 2002;38:79-94.
34. Lindberg I, Ahn SC, Breslin MB. Cellular distributions of the pro-hormone processing enzymes PC1 and PC2. Mol Cell Neurosci. 1994;5:614-622.
35. Teuchert M, Berghofer S, Klenk HD, Garten W. Recycling of furin from the plasma membrane. functional importance of the cyto-plasmic tail sorting signals and interaction with the AP-2 adaptor medium chain subunit. J Biol Chem. 1999;274:36781-36789.
36. Nour N, Mayer G, Mort JS, et al. The cysteine-rich domain of the secreted proprotein convertases PC5A and PACE4 functions as a cell surface anchor and interacts with tissue inhibitors of metallo-proteinases. Mol Biol Cell. 2005;16:5215-5226.
37. Tsuji A, Sakurai K, Kiyokage E, et al. Secretory proprotein conver-tases PACE4 and PC6A are heparin-binding proteins which are localized in the extracellular matrix. potential role of PACE4 in the activation of proproteins in the extracellular matrix. Biochim Biophys Acta. 2003;1645:95-104.
38. Egger M, Schgoer W, Beer AG, et al. Hypoxia up-regulates the angiogenic cytokine secretoneurin via an HIF-1alpha- and basic FGF-dependent pathway in muscle cells. FASEB J. 2007;21:2906-2917.
39. Tezel G, Wax MB. Hypoxia-inducible factor 1alpha in the glauco-matous retina and optic nerve head. Arch Ophthalmol. 2004;122: 1348-1356.
40. Mahloogi H, Bassi DE, Klein-Szanto AJ. Malignant conversion of non-tumorigenic murine skin keratinocytes overexpressing PACE4. Carcinogenesis. 2002;23:565-572.
41. McMahon S, Grondin F, McDonald PP, Richard DE, Dubois CM. Hypoxia-enhanced expression of the proprotein convertase furin is mediated by hypoxia-inducible factor-1: impact on the bioacti-vation of proproteins. J Biol Chem. 2005;280:6561-6569.
42. Bassi DE, Mahloogi H, Klein-Szanto AJ. The proprotein convertases furin and PACE4 play a significant role in tumor progression. Mol Carcinog. 2000;28:63-69.
43. Bassi DE, Mahloogi H, Al-Saleem L, de Lopez Cicco R, Ridge JA, Klein-Szanto AJ. Elevated furin expression in aggressive human head and neck tumors and tumor cell lines. Mol Carcinog. 2001; 31:224-232.
44. Bassi DE, de Lopez Cicco R, Cenna J, Litwin S, Cukierman E, Klein-Szanto AJ. PACE4 expression in mouse basal keratinocytes results in basement membrane disruption and acceleration of tumor progression. Cancer Res. 2005;65:7310-7319.
45. Nejjari M, Berthet V, Rigot V, et al. Inhibition of proprotein con-vertases enhances cell migration and metastases development of human colon carcinoma cells in a rat model. Am J Pathol. 2004; 164:1925-1933.
46. Wordinger RJ, Fleenor DL, Hellberg PE, et al. Effects of TGF-beta2, BMP-4, and gremlin in the trabecular meshwork: Implications for glaucoma. Invest Ophthalmol Vis Sci. 2007;48:1191-1200.
47. Lambert WS, Clark AF, Wordinger RJ. Effect of exogenous neuro-trophins on trk receptor phosphorylation, cell proliferation, and neurotrophin secretion by cells isolated from the human lamina cribrosa. Mol Vis. 2004;10:289-296.
48. Yang P, Hernandez MR. Purification of astrocytes from adult human optic nerve heads by immunopanning. Brain Res Brain Res Protoc. 2003;12:67-76.
49. Leitlein J, Aulwurm S, Waltereit R, et al. Processing of immunosuppressive pro-TGF-beta 1,2 by human glioblastoma cells involves cytoplasmic and secreted furin-like proteases. J Immunol. 2001; 166:7238-7243.
50. Paleyanda RK, Drews R, Lee TK, Lubon H. Secretion of human furin into mouse milk.JBiol Chem. 1997;272:15270-15274.
51. Cameron A, Appel J, Houghten RA, Lindberg I. Polyarginines are potent furin inhibitors.JBiol Chem. 2000;275:36741-36749.
52. Akamatsu T, Daikoku S, Nagamune H, et al. Developmental expression of a novel kexin family protease, PACE4E, in the rat olfactory system. Histochem Cell Biol. 1997;108:95-103.
53. Tsuji A, Higashine K, Hine C, et al. Identification of novel cDNAs encoding human kexin-like protease, PACE4 isoforms. Biochem Biophys Res Commun. 1994;200:943-950.
54. Zhong M, Benjannet S, Lazure C, Munzer S, Seidah NG. Functional analysis of human PACE4-A and PACE4-C isoforms: Identification of a new PACE4-CS isoform. FEBS Lett. 1996;396:31-36.
55. Tsuji A, Kanie H, Makise H, Yuasa K, Nagahama M, Matsuda Y. Engineering of alpha1-antitrypsin variants selective for subtilisin-like proprotein convertases PACE4 and PC6: Importance of the P2' residue in stable complex formation of the serpin with proprotein convertase. Protein Eng Des Sel. 2007;20:163-170.
56. Wang L, Cioffi GA, Cull G, Dong J, Fortune B. Immunohistologic evidence for retinal glial cell changes in human glaucoma. Invest Ophthalmol Vis Sci. 2002;43:1088-1094.
57. Varela HJ, Hernandez MR. Astrocyte responses in human optic nerve head with primary open-angle glaucoma.J Glaucoma. 1997; 6:303-313
58. Hernandez MR. The optic nerve head in glaucoma: role of astrocytes in tissue remodeling. Prog Retin Eye Res. 2000;19:297-321.
59. Tezel G, Hernandez MR, Wax MB. In vitro evaluation of reactive astrocyte migration, a component of tissue remodeling in glaucomatous optic nerve head. Glia. 2001;34:178-189.
60. Agapova OA, Kaufman PL, Lucarelli MJ, Gabelt BT, Hernandez MR. Differential expression of matrix metalloproteinases in monkey eyes with experimental glaucoma or optic nerve transection. Brain Res. 2003;967:132-143
61. Agapova OA, Ricard CS, Salvador-Silva M, Hernandez MR. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human optic nerve head astrocytes. Glia. 2001;33: 205-216.
62. He S, Prasanna G, Yorio T. Endothelin-1-mediated signaling in the expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in astrocytes. Invest Ophthalmol Vis Sci. 2007; 48:3737-3745.
63. Johnson EC, Jia L, Cepurna WO, Doser TA, Morrison JC. Global changes in optic nerve head gene expression after exposure to elevated intraocular pressure in a rat glaucoma model. Invest Ophthal mol Vis Sci. 2007;48:3161-3177.
64. Pena JD, Taylor AW, Ricard CS, Vidal I, Hernandez MR. Transforming growth factor beta isoforms in human optic nerve heads. Br J Ophthalmol. 1999;83:209-218.
65. Lambert W, Agarwal R, Howe W, Clark AF, Wordinger RJ. Neurotrophin and neurotrophin receptor expression by cells of the human lamina cribrosa. Invest Ophthalmol Vis Sci. 2001;42:2315-2323.
66. Lambert WS, Clark AF, Wordinger RJ. Neurotrophin and trk expression by cells of the human lamina cribrosa following oxygen-glucose deprivation. BMC Neurosci. 2004;5:51
67. Lee R, Kermani P, Teng KK, Hempstead BL. Regulation of cell survival by secreted proneurotrophins. Science. 2001;294:1945-1948.
68. Fahnestock M, Michalski B, Xu B, Coughlin MD. The precursor pro-nerve growth factor is the predominant form of nerve growth factor in brain and is increased in Alzheimer's disease. Mol Cell Neurosci. 2001;18:210-220.
69. Peng S, Wuu J, Mufson EJ, Fahnestock M. Increased proNGF levels in subjects with mild cognitive impairment and mild alzheimer disease.JNeuropathol Exp Neurol. 2004;63:641-649
70. Harrington AW, Leiner B, Blechschmitt C, et al. Secreted proNGF is a pathophysiological death-inducing ligand after adult CNS injury. Proc Natl Acad Sci USA. 2004;101:6226-6230.
71. Teng HK, Teng KK, Lee R, et al. ProBDNF induces neuronal apoptosis via activation of a receptor complex of p75NTR and sortilin. J Neurosci. 2005;25:5455-5463.
72. Cuello AC, Bruno MA. The failure in NGF maturation and its increased degradation as the probable cause for the vulnerability of cholinergic neurons in alzheimer's disease. Neurochem Res. 2007;32:1041-1045.
73. Bierl MA, Isaacson LG. Increased NGF proforms in aged sympathetic neurons and their targets. Neurobiol Aging. 2007;28:122-134.
74. Bruno MA, Cuello AC. Activity-dependent release of precursor nerve growth factor, conversion to mature nerve growth factor, and its degradation by a protease cascade. Proc Natl Acad Sci USA. 2006;103:6735-6740.
75. Constam DB, Calfon M, Robertson EJ. SPC4, SPC6, and the novel protease SPC7 are coexpressed with bone morphogenetic proteins at distinct sites during embryogenesis.JCell Biol. 1996;134: 181-191
76. Constam DB, Robertson EJ. SPC4/PACE4 regulates a TGFbeta signaling network during axis formation. Genes Dev. 2000;14:1146-1155
77. Guo L, Moss SE, Alexander RA, Ali RR, Fitzke FW, Cordeiro MF. Retinal ganglion cell apoptosis in glaucoma is related to intraocular pressure and IOP-induced effects on extracellular matrix. Invest Ophthalmol Vis Sci. 2005;46:175-182.
78. Lutjen-Drecoll E. Morphological changes in glaucomatous eyes and the role of TGFbeta2 for the pathogenesis of the disease. Exp Eye Res. 2005;81:1-4.
79. Fuchshofer R, Birke M, Welge-Lussen U, Kook D, Lutjen-Drecoll E. Transforming growth factor-beta 2 modulated extracellular matrix component expression in cultured human optic nerve head astrocytes. Invest Ophthalmol Vis Sci. 2005;46:568-578.
80. Neumann C, Yu A, Welge-Lussen U, Lutjen-Drecoll E, Birke M. The effect of TGF-/32 on elastin, type VI collagen, and components of the proteolytic degradation system in human optic nerve astrocytes. Invest Ophthalmol Vis Sci. 2008;49:1464-1472.
81. Kusakabe M, Cheong PL, Nikfar R, McLennan IS, Koishi K. The structure of the TGF-beta latency associated peptide region determines the ability of the proprotein convertase furin to cleave TGF-betas. J Cell Biochem. 2008;103:311-320.
82. Dubois CM, Blanchette F, Laprise MH, Leduc R, Grondin F, Seidah NG. Evidence that furin is an authentic transforming growth factor-beta1-converting enzyme. Am J Pathol. 2001;158:305-316.
83. Dubois CM, Laprise MH, Blanchette F, Gentry LE, Leduc R. Processing of transforming growth factor beta 1 precursor by human furin convertase. J Biol Chem. 1995;270:10618-10624.